Short-term exercise training improves cardiac function associated to a better antioxidant response and lower type 3 iodothyronine deiodinase activity after myocardial infarction
Autoři:
Rafael Aguiar Marschner aff001; Patrícia Banda aff001; Simone Magagnin Wajner aff002; Melissa Medeiros Markoski aff003; Maximiliano Schaun aff001; Alexandre Machado Lehnen aff001
Působiště autorů:
Institute of Cardiology of Rio Grande do Sul/University Foundation of Cardiology, Porto Alegre, Rio Grande do Sul, Brazil
aff001; Thyroid Division, Endocrinology Service, Hospital de Clínicas de Porto Alegre/Federal University of Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil
aff002; Federal University of Health Sciences of Porto Alegre, Porto Alegre, Rio Grande do Sul, Brazil
aff003
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222334
Souhrn
Aims
We assessed the effects of a short-term exercise training on cardiac function, oxidative stress markers, and type 3 iodothyronine deiodinase (D3) activity in cardiac tissue of spontaneously hypertensive rats (SHR) following experimental myocardial infarction (MI).
Methods
Twenty-four SHR (aged 3 months) were allocated to 4 groups: sham+sedentary, sham+trained, MI+sedentary and MI+trained. MI was performed by permanent ligation of the coronary artery. Exercise training (treadmill) started 96 hours after MI and lasted for 4 weeks (~60% maximum effort, 4x/week and 40 min/day). Cardiac function (echocardiography), thioredoxin reductase (TRx), total carbonyl levels, among other oxidative stress markers and D3 activity were measured. A Generalized Estimating Equation was used, followed by Bonferroni’s test (p<0.05).
Results
MI resulted in an increase in left ventricular mass (p = 0.002) with decreased cardiac output (~22.0%, p = 0.047) and decreased ejection fraction (~41%, p = 0.008) as well as an increase in the carbonyl levels (p = 0.001) and D3 activity (~33%, p<0.001). Exercise training resulted in a decrease in left ventricular mass, restored cardiac output (~34%, p = 0.048) and ejection fraction (~20%, p = 0.040), increased TRx (~85%, p = 0.007) and reduced carbonyl levels (p<0.001) and D3 activity (p<0.001).
Conclusions
Our short-term exercise training helped reverse the effects of MI on cardiac function. These benefits seem to derive from a more efficient antioxidant response and lower D3 activity in cardiac tissue.
Klíčová slova:
Biology and life sciences – Cell biology – Biochemistry – Physical sciences – Chemistry – Chemical reactions – Medicine and health sciences – Physiology – Public and occupational health – Physical activity – Cardiology – Sports science – Sports and exercise medicine – Exercise – Physical fitness – Antioxidants – Oxidative stress – Electrochemistry – Myocardial infarction – Cardiac output – Cardiovascular physiology – Peptides – Glutathione – Oxidation-reduction reactions
Zdroje
1. Al-Gubory KH, Fowler PA, Garrel C. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell Biol. 2010;42(10):1634–1650. doi: 10.1016/j.biocel.2010.06.001 20601089
2. Wassen FW, Schiel AE, Kuiper GG, Kaptein E, Bakker O, Visser TJ, Simonides WS. Induction of thyroid hormone-degrading deiodinase in cardiac hypertrophy and failure. Endocrinology. 2002;143(7):2812–2815. 12072417
3. Lehnen TE, Santos MV, Lima A, Maia AL, Wajner SM. N-Acetylcysteine Prevents Low T3 Syndrome and Attenuates Cardiac Dysfunction in a Male Rat Model of Myocardial Infarction. Endocrinology. 2017;158(5):1502–1510. doi: 10.1210/en.2016-1586 28323971
4. Pol CJ, Muller A, Zuidwijk MJ, van Deel ED, Kaptein E, Saba A, Marchini M, Zucchi R, Visser TJ, Paulus WJ, Duncker DJ, Simonides WS. Left-ventricular remodeling after myocardial infarction is associated with a cardiomyocyte-specific hypothyroid condition. Endocrinology. 2011;152(2):669–679. doi: 10.1210/en.2010-0431 21159857
5. Pol CJ, Muller A, Simonides WS. Cardiomyocyte-specific inactivation of thyroid hormone in pathologic ventricular hypertrophy: an adaptative response or part of the problem? Heart Fail Rev. 2010;15(2):133–142. doi: 10.1007/s10741-008-9133-7 19107595
6. Schaun MI, Marschner RA, Peres TR, Markoski MM, Lehnen AM. Aerobic training prior to myocardial infarction increases cardiac GLUT4 and partially preserves heart function in spontaneously hypertensive rats. Appl Physiol Nutr Metab. 2017;42(3):334–337. doi: 10.1139/apnm-2016-0439 28177731
7. Garza MA, Wason EA, Zhang JQ. Cardiac remodeling and physical training post myocardial infarction. World J Cardiol. 2015;7(2):52–64. doi: 10.4330/wjc.v7.i2.52 25717353
8. Schaun MI, Motta LL, Teixeira R, Klamt F, Rossato J, Lehnen AM, Irigoyen MC, Markoski M. Preventive Physical Training Partially Preserves Heart Function and Improves Cardiac Antioxidant Responses in Rats After Myocardial Infarction. Int J Sport Nutr Exerc Metab. 2017:1–20.
9. Seifi-Skishahr F, Damirchi A, Farjaminezhad M, Babaei P. Physical Training Status Determines Oxidative Stress and Redox Changes in Response to an Acute Aerobic Exercise. Biochem Res Int. 2016;2016:3757623. doi: 10.1155/2016/3757623 27064342
10. Wajner SM, Maia AL. New Insights toward the Acute Non-Thyroidal Illness Syndrome. Front Endocrinol (Lausanne). 2012;3:8.
11. Leosco D, Rengo G, Iaccarino G, Golino L, Marchese M, Fortunato F, Zincarelli C, Sanzari E, Ciccarelli M, Galasso G, Altobelli GG, Conti V, Matrone G, Cimini V, Ferrara N, Filippelli A, Koch WJ, Rengo F. Exercise promotes angiogenesis and improves beta-adrenergic receptor signalling in the post-ischaemic failing rat heart. Cardiovasc Res. 2008;78(2):385–394. 18093988
12. Miyachi M, Yazawa H, Furukawa M, Tsuboi K, Ohtake M, Nishizawa T, Hashimoto K, Yokoi T, Kojima T, Murate T, Yokota M, Murohara T, Koike Y, Nagata K. Exercise training alters left ventricular geometry and attenuates heart failure in dahl salt-sensitive hypertensive rats. Hypertension. 2009;53(4):701–707. doi: 10.1161/HYPERTENSIONAHA.108.127290 19255362
13. Folkman J. Seminars in Medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. N Engl J Med. 1995;333(26):1757–1763. 7491141
14. Swaminathan JK, Khan M, Mohan IK, Selvendiran K, Niranjali Devaraj S, Rivera BK, Kuppusamy P. Cardioprotective properties of Crataegus oxycantha extract against ischemia-reperfusion injury. Phytomedicine. 2010;17(10):744–752. doi: 10.1016/j.phymed.2010.01.009 20171068
15. Pfeffer J, Pfeffer M, MC F, ED F. Cardiac function and morphology with aging in the spontaneously hypertensive rat. Am J Physiol. 1979;237(4):H461–468. 495731
16. Lehnen TE, Lehnen AM, Tavares AM, Bello-Klein A, Markoski MM, Machado UF, Schaan B. Atorvastatin administered before myocardial infarction in rats improves contractility irrespective of metabolic changes. Clin Exp Pharmacol Physiol. 2014;41(12):986–994. doi: 10.1111/1440-1681.12313 25223307
17. Nozawa E, Kanashiro RM, Murad N, Carvalho AC, Cravo SL, Campos O, Tucci PJ, Moises VA. Performance of two-dimensional Doppler echocardiography for the assessment of infarct size and left ventricular function in rats. Braz J Med Biol Res. 2006;39(5):687–695. 16648907
18. Peron AP, Saraiva RM, Antonio EL, Tucci PJ. Mechanical function is normal in remanent myocardium during the healing period of myocardial infarction—despite congestive heart failure. Arq Bras Cardiol. 2006;86(2):105–112. 16501801
19. Caponi PW, Lehnen AM, Pinto GH, Borges J, Markoski M, Machado UF, Schaan BD. Aerobic exercise training induces metabolic benefits in rats with metabolic syndrome independent of dietary changes. Clinics (Sao Paulo). 2013;68(7):1010–1017.
20. Lehnen AM, Leguisamo NM, Pinto GH, Markoski M, De Angelis K, Machado UF, Schaan B. Exercise-stimulated GLUT4 expression is similar in normotensive and hypertensive rats. Horm Metab Res. 2011;43(4):231–235. doi: 10.1055/s-0031-1271747 21332027
21. Lehnen AM, Leguisamo NM, Pinto GH, Markoski MM, De Angelis K, Machado UF, Schaan B. The beneficial effects of exercise in rodents are preserved after detraining: a phenomenon unrelated to GLUT4 expression. Cardiovasc Diabetol. 2010;9:67. doi: 10.1186/1475-2840-9-67 21029425
22. Teare JP, Punchard NA, Powell JJ, Lumb PJ, Mitchell WD, Thompson RP. Automated spectrophotometric method for determining oxidized and reduced glutathione in liver. Clin Chem. 1993;39(4):686–689. 8472367
23. Zanatta A, Viegas CM, Tonin AM, Busanello EN, Grings M, Moura AP, Leipnitz G, Wajner M. Disturbance of redox homeostasis by ornithine and homocitrulline in rat cerebellum: a possible mechanism of cerebellar dysfunction in HHH syndrome. Life Sci. 2013;93(4):161–168. doi: 10.1016/j.lfs.2013.06.013 23806752
24. Huang SA, Mulcahey MA, Crescenzi A, Chung M, Kim BW, Barnes C, Kuijt W, Turano H, Harney J, Larsen PR. Transforming growth factor-beta promotes inactivation of extracellular thyroid hormones via transcriptional stimulation of type 3 iodothyronine deiodinase. Mol Endocrinol. 2005;19(12):3126–3136. 16037131
25. Wajner SM, Goemann IM, Bueno AL, Larsen PR, Maia AL. IL-6 promotes nonthyroidal illness syndrome by blocking thyroxine activation while promoting thyroid hormone inactivation in human cells. J Clin Invest. 2011;121(5):1834–1845. doi: 10.1172/JCI44678 21540553
26. dos Santos L, Santos AA, Goncalves GA, Krieger JE, Tucci PJ. Bone marrow cell therapy prevents infarct expansion and improves border zone remodeling after coronary occlusion in rats. Int J Cardiol. 2010;145(1):34–39. doi: 10.1016/j.ijcard.2009.06.008 19577315
27. Tucci PJ. Pathophysiological characteristics of the post-myocardial infarction heart failure model in rats. Arq Bras Cardiol. 2011;96(5):420–424. 21503387
28. Wan W, Powers AS, Li J, Ji L, Erikson JM, Zhang JQ. Effect of post-myocardial infarction exercise training on the renin-angiotensin-aldosterone system and cardiac function. Am J Med Sci. 2007;334(4):265–273. 18030183
29. De Angelis K, Wichi RB, Jesus WR, Moreira ED, Morris M, Krieger EM, Irigoyen MC. Exercise training changes autonomic cardiovascular balance in mice. J Appl Physiol (1985). 2004;96(6):2174–2178.
30. Petriz BA, Almeida JA, Gomes CP, Ernesto C, Pereira RW, Franco OL. Exercise performed around MLSS decreases systolic blood pressure and increases aerobic fitness in hypertensive rats. BMC Physiol. 2015;15:1. doi: 10.1186/s12899-015-0015-7 25888441
31. Davies KJ, Quintanilha AT, Brooks GA, Packer L. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun. 1982;107(4):1198–1205. 6291524
32. Steinbacher P, Eckl P. Impact of oxidative stress on exercising skeletal muscle. Biomolecules. 2015;5(2):356–377. doi: 10.3390/biom5020356 25866921
33. Linke A, Adams V, Schulze PC, Erbs S, Gielen S, Fiehn E, Mobius-Winkler S, Schubert A, Schuler G, Hambrecht R. Antioxidative effects of exercise training in patients with chronic heart failure: increase in radical scavenger enzyme activity in skeletal muscle. Circulation. 2005;111(14):1763–1770. 15809365
34. Muthusamy VR, Kannan S, Sadhaasivam K, Gounder SS, Davidson CJ, Boeheme C, Hoidal JR, Wang L, Rajasekaran NS. Acute exercise stress activates Nrf2/ARE signaling and promotes antioxidant mechanisms in the myocardium. Free Radic Biol Med. 2012;52(2):366–376. doi: 10.1016/j.freeradbiomed.2011.10.440 22051043
35. Meister A, Anderson ME. Glutathione. Annu Rev Biochem. 1983;52:711–760. 6137189
36. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev. 2008;88(4):1243–1276. doi: 10.1152/physrev.00031.2007 18923182
37. Yamamoto M, Yang G, Hong C, Liu J, Holle E, Yu X, Wagner T, Vatner SF, Sadoshima J. Inhibition of endogenous thioredoxin in the heart increases oxidative stress and cardiac hypertrophy. J Clin Invest. 2003;112(9):1395–1406. doi: 10.1172/JCI17700 14597765
38. Yang Y, Ago T, Zhai P, Abdellatif M, Sadoshima J. Thioredoxin 1 negatively regulates angiotensin II-induced cardiac hypertrophy through upregulation of miR-98/let-7. Circ Res. 2011;108(3):305–313. doi: 10.1161/CIRCRESAHA.110.228437 21183740
39. Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD, Vatner SF, Sadoshima J. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell. 2008;133(6):978–993. doi: 10.1016/j.cell.2008.04.041 18555775
40. Liu Y, Cox SR, Morita T, Kourembanas S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5' enhancer. Circ Res. 1995;77(3):638–643. 7641334
41. Pinho CA, Tromm CB, Tavares AM, Silva LA, Silveira PC, Souza CT, Benetti M, Pinho RA. Effects of different physical training protocols on ventricular oxidative stress parameters in infarction-induced rats. Life Sci. 2012;90(13–14):553–559. doi: 10.1016/j.lfs.2012.01.018 22365960
42. Holloway TM, Bloemberg D, da Silva ML, Simpson JA, Quadrilatero J, Spriet LL. High intensity interval and endurance training have opposing effects on markers of heart failure and cardiac remodeling in hypertensive rats. PLoS One. 2015;10(3):e0121138. doi: 10.1371/journal.pone.0121138 25803693
43. Maia AL, Goemann IM, Meyer EL, Wajner SM. Deiodinases: the balance of thyroid hormone: type 1 iodothyronine deiodinase in human physiology and disease. J Endocrinol. 2011;209(3):283–297. 21415143
44. Simonides WS, Mulcahey MA, Redout EM, Muller A, Zuidwijk MJ, Visser TJ, Wassen FW, Crescenzi A, da-Silva WS, Harney J, Engel FB, Obregon MJ, Larsen PR, Bianco AC, Huang SA. Hypoxia-inducible factor induces local thyroid hormone inactivation during hypoxic-ischemic disease in rats. J Clin Invest. 2008;118(3):975–983. doi: 10.1172/JCI32824 18259611
45. Lesmana R, Iwasaki T, Iizuka Y, Amano I, Shimokawa N, Koibuchi N. The change in thyroid hormone signaling by altered training intensity in male rat skeletal muscle. Endocr J. 2016;63(8):727–738. doi: 10.1507/endocrj.EJ16-0126 27350720
46. Steinacker JM, Brkic M, Simsch C, Nething K, Kresz A, Prokopchuk O, Liu Y. Thyroid hormones, cytokines, physical training and metabolic control. Horm Metab Res. 2005;37(9):538–544. 16175490
47. Danzi S, Klein I. Thyroid hormone-regulated cardiac gene expression and cardiovascular disease. Thyroid. 2002;12(6):467–472. 12165108
48. Olivares EL, Marassi MP, Fortunato RS, da Silva AC, Costa-e-Sousa RH, Araujo IG, Mattos EC, Masuda MO, Mulcahey MA, Huang SA, Bianco AC, Carvalho DP. Thyroid function disturbance and type 3 iodothyronine deiodinase induction after myocardial infarction in rats a time course study. Endocrinology. 2007;148(10):4786–4792. 17628010
49. Redout EM, van der Toorn A, Zuidwijk MJ, van de Kolk CW, van Echteld CJ, Musters RJ, van Hardeveld C, Paulus WJ, Simonides WS. Antioxidant treatment attenuates pulmonary arterial hypertension-induced heart failure. Am J Physiol Heart Circ Physiol. 2010;298(3):H1038–1047. doi: 10.1152/ajpheart.00097.2009 20061549
50. Iervasi G, Pingitore A, Landi P, Raciti M, Ripoli A, Scarlattini M, L’Abbate A, Donato L. sLow-T3 syndrome: a strong prognostic predictor of death in patients with heart disease. Circulation. 2003;107(5):708–713.
51. Vidart J, Wajner SM, Leite RS, Manica A, Schaan BD, Larsen PR, Maia AL. N-acetylcysteine administration prevents nonthyroidal illness syndrome in patients with acute myocardial infarction: a randomized clinical trial. J Clin Endocrinol Metab. 2014;99(12):4537–4545. doi: 10.1210/jc.2014-2192 25148231
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania